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Zanolli, Clément and Bayle, Priscilla and Bondioli, Luca and Dean, Christopher and Le Luyer,Mona and Mazurier, Arnaud and Morita, Wataru and Macchiarelli, Roberto (2017) Is the deciduous/permanentmolar enamel thickness ratio a taxon-specific indicator in extant and extinct hominids? ComptesRendus Palevol, 16 (5-6). pp. 702-714. ISSN 1631-0683.

DOI

https://doi.org/10.1016/j.crpv.2017.05.002

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http://kar.kent.ac.uk/62148/

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C. R. Palevol 16 (2017) 702–714

Contents lists available at ScienceDirect

Comptes Rendus Palevol

www.sc iencedi rec t .com

Human Palaeontology and Prehistory

Is the deciduous/permanent molar enamel thickness ratio ataxon-specific indicator in extant and extinct hominids?

Le rapport d’épaisseur de l’émail des molaires déciduales/permanentes

est-il un indicateur taxinomique chez les hominidés actuels et fossiles ?

Clément Zanolli a,∗, Priscilla Bayleb, Luca Bondioli c, M. Christopher Deand,Mona Le Luyerb,e, Arnaud Mazurier f, Wataru Moritag, Roberto Macchiarellih,i

a UMR 5288 CNRS, Laboratoire AMIS, Université Toulouse-3 Paul-Sabatier, 31062 Toulouse, Franceb UMR 5199 CNRS, Laboratoire PACEA, Université de Bordeaux, 33615 Bordeaux, Francec Sezione di Bioarcheologia, Museo Nazionale Preistorico Etnografico “Luigi Pigorini”, Rome, Italyd Department of Cell and Developmental Biology, University College London, London WC1E 6BT, UKe School of Anthropology & Conservation, University of Kent, Canterbury, UKf UMR 7285 CNRS, Institut de chimie des milieux et matériaux de Poitiers, Université de Poitiers, 86073 Poitiers, Franceg Department of Oral Functional Anatomy, Graduate School of Dental Medicine, Hokkaido University, Hokkaido, Japanh UMR 7194 CNRS, Laboratoire HNHP, Muséum national d’histoire naturelle, 75116 Paris, Francei Unité de formation Géosciences, Université de Poitiers, 86073 Poitiers, France

a r t i c l e i n f o

Article history:

Received 7 April 2017Accepted after revision 4 May 2017Available online 16 June 2017

Handled by Roberto Macchiarelli and

Clément Zanolii

Keywords:

EnamelDm2M1“Diphyodontic index”Hominids

a b s t r a c t

In Primates, enamel thickness variation stems from an evolutionary interplay betweenfunctional/adaptive constraints (ecology) and the strict control mechanisms of the mor-phogenetic program. Most studies on primate enamel thickness have primarily consideredthe permanent teeth, while the extent of covariation in tooth enamel thickness distribu-tion between deciduous and permanent counterparts remains poorly investigated. In thistest study on nine extant and fossil hominids we investigated the degree of covariationin enamel proportions between 25 pairs of mandibular dm2 and M1 by a so-called “lat-eral enamel thickness diphyodontic index”. The results did not provide an unambiguouspicture, but rather suggest complex patterns likely resulting from the influence of manyinteractive factors. Future research should test the congruence of the “diphyodontic signal”between the anterior and the postcanine dentition, as well as between enamel and theenamel-dentine junction topography.

© 2017 Academie des sciences. Published by Elsevier Masson SAS. All rights reserved.

Mots clés :

ÉmailDm2M1« Indice diphyodonte »

Hominidés

r é s u m é

Chez les primates, le patron de variation d’épaisseur de l’émail est issu d’un compro-mis évolutif entre contraintes fonctionnelles/adaptatives (écologiques) et mécanismes decontrôle morphogénétique. La majorité des études portant sur l’épaisseur de l’émail desprimates concerne les dents permanentes, tandis que le degré de covariation de distri-bution d’épaisseur de l’émail entre les équivalents déciduaux et permanents reste encore

∗ Corresponding author.E-mail address: clement.zanolli@gmail.com (C. Zanolli).

http://dx.doi.org/10.1016/j.crpv.2017.05.0021631-0683/© 2017 Academie des sciences. Published by Elsevier Masson SAS. All rights reserved.

C. Zanolli et al. / C. R. Palevol 16 (2017) 702–714 703

méconnu. Dans cette étude préliminaire, nous explorons le degré de covariation des pro-portions d’émail entre 25 paires de dm2 et M1 mandibulaires de neuf hominidés actuels etfossiles en élaborant un « indice diphyodonte d’épaisseur de l’émail latéral ». Les résultatsne montrent pas un signal évident, mais suggèrent plutôt des modèles complexes résultantprobablement de l’influence d’interactions entre des facteurs variés. De futures recherchessur le sujet devraient tester le degré de congruence du « signal diphyodonte » entre lesdents antérieures et post-canines, ainsi qu’entre l’émail et la topographie de la jonctionémail–dentine.

© 2017 Academie des sciences. Publie par Elsevier Masson SAS. Tous droits reserves.

1. Introduction

Following the pioneering methodological work devel-oped by L.B. Martin for measurement procedure andstandardization (Martin, 1985), the bi-three-dimensionalassessment of tooth enamel thickness has become routinein taxonomic and adaptive/evolutionary studies of fossiland extant primates (e.g., Alba et al., 2013; Kono, 2004;Kono et al., 2014; Macchiarelli et al., 2004, 2009, 2013;Olejniczak et al., 2008a, 2008b, 2008c, 2008d; Pan et al.,2016; Skinner et al., 2015; Smith et al., 2003, 2005, 2011,2012; Suwa et al., 2009; Zanolli et al., 2015, 2016a). Com-monly used to infer durophagy and considered as a proxyof the dietary niches exploited by extinct species (e.g.,Constantino et al., 2011, 2012; Lucas et al., 2008; Martinet al., 2003; Schwartz, 2000a; Teaford, 2007; Teaford andUngar, 2015; Vogel et al., 2008), occlusal enamel thicknessis seen as intimately related to dietary abrasiveness andselectively responsive to lifetime dental wear resistance(Pampush et al., 2013; Rabenold and Pearson, 2011).

In primates, enamel thickness variation stems from anevolutionary interplay between functional/adaptive con-straints (ecology) and strict control mechanisms of themorphogenetic program (Horvath et al., 2014; Kelley andSwanson, 2008; Kono, 2004; Simmer et al., 2010; Smithet al., 2012; Vogel et al., 2008). It appears to respond rel-atively quickly in evolutionary time to dietary/ecologicalchanges (Grine and Daegling, 2017; Hlusko et al., 2004;Le Luyer and Bayle, 2017), thus being prone to homoplasy(Smith et al., 2012; rev. in Macho, 2015).

Most studies on enamel thickness have primarily con-sidered the permanent teeth, especially the molar series,while the extent of covariation in tooth enamel thick-ness between deciduous and permanent counterparts hasbeen the object of limited quantitative analyses, includ-ing in hominids (for a recent synthesis and review ofstudies on deciduous enamel thickness in humans, seetable 1 in Mahoney, 2013; additionally, among other con-tributions, see Benazzi et al., 2011; Fornai et al., 2014,2016; Macchiarelli et al., 2006, 2013; Peretto et al.,2015; Zanolli, 2015a; Zanolli et al., 2010a, 2012, 2014).Accordingly, quantitative support to answer a number ofquestions remains so far elusive. More specifically: when-ever, in a comparative intertaxonomic assessment, wescore a permanent hominid tooth as relatively “thinly”-or “thickly-enamelled” and order it accordingly within aseries of investigated specimens, does the primary elementscore similarly and does it (tend to) occupy a compara-ble position within the same deciduous series? Can we

confidently predict an enamel thickness “category” fora hominid deciduous crown based on the measure ofthe permanent tooth (or vice versa)? Does a predictabledeciduous-permanent pattern exist for tooth enamel thick-ness in hominids? If so, is it taxon-specific?

The second deciduous (dm2) and the first permanent(M1) molars are part of the same developmental molarseries (rev. in Bailey et al., 2014, 2016; see also Evanset al., 2016), i.e., they are meristic elements with a similarand serially repeated structure within the same organ-ism (Butler, 1956, 1967; Kraus and Jordan, 1965). In thisstudy on some extant and fossil hominids, we thus inves-tigate the degree of covariation in enamel proportionsbetween the dm2 and the M1 (for the extant human con-dition, see Gantt et al., 2001; Grine, 2005; Huszár, 1972;Mahoney, 2010; Rossi et al., 1999). In order to performintertaxonomic comparisons, we established a so-called“lateral enamel thickness diphyodontic index” (LETDI; see§ Materials and methods) as a measure of the propor-tions in the amount of non-occlusal enamel (Macchiarelliet al., 2016; Zanolli, 2015b). Even if the mandibular dm2and the M1 specifically used in this study are not suc-cessional elements, we introduced the wider concept of“diphyodontic index” referring to their usual differentialuse-life. Given the exploratory nature of this study, whosemain goal is to capture a tendency or trend, if any, andnot to assess intraspecific variation, or evolutionary trends,or phylogenetic relationships, the number of cases exam-ined for each taxon (ranging from 1 to 5 tooth pairs) isjust minimal. By definition, at this stage of the research theunderlying assumption is that the signal revealed by eachdm2-M1 crown pair used here, all from mandibular den-titions, represents the average condition of its own taxon,i.e., is taxon-representative.

Apart from some intertaxonomic differences in devel-opmental timing and patterning between the dm2 and theM1 (Dean, 2000, 2006, 2010; Dean and Cole, 2013), giventhat the dm2 is in functional occlusion for a much shortertime and commonly experiences lower functional con-straints at least until the weaning process begins (Fleagle,2013; Swindler, 2002), we expect that, independentlyfrom their relative qualitative “category” (“thinner” vs.“thicker”), the dm2/M1 enamel relative volume ratiosare < 1.

2. Materials and methods

The hominid taxa considered in this study includethe four extant genera Homo (HOM), Pan (PAN), Gorilla

704 C. Zanolli et al. / C. R. Palevol 16 (2017) 702–714

Table 1

List of the extant and fossil hominid taxa considered in the present study with their lateral enamel proportions of the second deciduous (dm2) and firstpermanent (M1) lower molars.Tableau 1

Liste des taxons hominidés actuels et fossiles considérés dans la présente étude avec les proportions d’émail latéral des secondes molaires déciduales (dm2)et des premières molaires permanentes (M1) mandibulaires.

Label N crowns (specimens) Collection/site References

Extant taxaHomo HOM 5 dm2s – 5 M1s MNPELP; PBC Original dataPan PAN 4 dm2s – 4 M1s Univ. Poitiers & Univ.

Toulouse, FranceOriginal data

Gorilla GOR 5 dm2s – 5 M1s Univ. Poitiers & Univ.Toulouse, France

Original data

Pongo PON 4 dm2s – 4 M1s MZS; Univ. Toulouse,France

Original data

Fossil taxaNeanderthals Nea 3 dm2s (RdM, S14–5, S42)

3 M1s (RdM, S14–7, S49)Roc de Marsal (RdM) andAbri Suard (S), France

Bayle, 2008; Bayle et al.,2009; Macchiarelli et al.,2006; NESPOS Database,2017

Paranthropus robustus PAR 1 dm2 – 1 M1 (SK 63) Swartkrans, South Africa Original dataAustralopithecus africanus AUS 1 dm2 – 1 M1 (STS 24) Sterkfontein, South Africa Original dataOuranopithecus macedoniensis OUR 1 dm2 – 1 M1 (RPL–83) Ravin de la Pluie,

Macedonia, GreeceMacchiarelli et al., 2009

Oreopithecus bambolii ORE 1 dm2 (FS1995#0009)1 M1 (FS1996#Fi98)

Fiume Santo, Sardinia, Italy Zanolli et al., 2010b, 2016a

MNPELP: Museo Nazionale Preistorico Etnografico “L. Pigorini”, Rome, Italy; PBC: Pretoria Bone Collection, University of Pretoria, South Africa; MZS: Muséezoologique, Strasbourg, France.

(GOR) and Pongo (PON), and representatives of four fossilgenera: the Plio-Pleistocene hominins Paranthropus (robus-

tus) (PAR) and Australopithecus (africanus) (AUS), from theSouth African sites of Swartkrans and Sterkfontein, respec-tively, and the late Miocene European apes Ouranopithecus

(macedoniensis) (OUR), from Macedonia, and Oreopithecus

(bambolii) (ORE), from Sardinia. Besides H. sapiens, humansare also represented by the extinct Neanderthals (Nea).The existence of interspecific differences in molar enamelthickness has been ascertained within the australopithclade (e.g., Grine and Daegling, 2017; Grine and Martin,1988; Olejniczak et al., 2008b; Pan et al., 2016; Skinneret al., 2015), but their consideration here is far beyond thespecific purposes of our present work.

Details about the composition and origin of themandibular dm2 and M1 specimens/samples are providedin Table 1. The extant human teeth, all from individ-uals of European origins, represent both sexes; conversely,no detailed information, including about their geographicprovenance (and if from captive or wild individuals), isavailable to us regarding the extant great ape representa-tives. All pairs examined here are from single individuals,except for Oreopithecus. Because of the paucity of fossilmaterials suitable for such kind of analyses and the evenmore scanty number of currently available/accessible high-resolution records detailing the hominid tooth crown innerstructure, in this first study we preferred to maximize theamount of signals, especially at generic level.

We have used the X-ray microtomographic record avail-able to us of specimens which have been previouslyscanned at: the University of Poitiers, France, by a ViscomX8050-16 system (all extant taxa; original data); the ID 17beam line of the European Synchrotron Radiation Facilityof Grenoble, France (Neanderthals and Oreopithecus; Bayle,2008; Bayle et al., 2009; Macchiarelli et al., 2006; NESPOS

Database, 2017; Zanolli et al., 2010b, 2016a); the SouthAfrican Nuclear Energy Corporation (Necsa), Pelindaba, bya Nikon XTH 225 ST equipment (Paranthropus and Aus-

tralopithecus; original data); and the analytical platform setat the Bundesanstalt für Materialforschung und -prüfung(BAM) of Berlin, Germany (Ouranopithecus; Macchiarelliet al., 2008, 2009).

The data were reconstructed at a voxel size ranging from21.0 to 83.2 �m, for the extant teeth, and from 21.6 to50.0 �m, for the fossil specimens. Using Amira v.5.3 (Visu-alization Sciences Group Inc.) and ImageJ v.1.46 (Schneideret al., 2012), a semiautomatic threshold-based segmenta-tion was carried out following the half-maximum heightmethod (HMH; Spoor et al., 1993) and the region of interestthresholding protocol (ROI-Tb; Fajardo et al., 2002), takingrepeated measurements on different slices of the virtualstack (Coleman and Colbert, 2007).

In order to avoid the problem of occlusal wear nearlyinvariably affecting at least the dm2 in most molar pairs,we uniquely considered lateral enamel. As lateral enamelthickness topography has a profound effect on crownmorphology, it is expected to bring a taxon-specific sig-nature, even if likely diluted compared to that providedby total enamel thickness that includes occlusal enamel(e.g., Kono and Suwa, 2008; Macchiarelli et al., 2013;Suwa et al., 2009). To quantify lateral enamel, the best-fit plane across the cervicoenamel line was firstly seton each crown and the tooth material below this basalplane eliminated (Olejniczak et al., 2008a). Then, a paral-lel plane to the former, tangent to the lowest enamel pointof the occlusal basin, was defined and all material aboveit was also removed (Macchiarelli et al., 2013; Toussaintet al., 2010). Only the enamel and dentine portionsbetween these two planes was preserved to estimate tissueproportions.

C. Zanolli et al. / C. R. Palevol 16 (2017) 702–714 705

On the new set of virtually reduced and simplifiedcrowns, five surface and volumetric variables were dig-itally measured (or calculated): LVe, the lateral volumeof enamel (mm3); LVcdp, the lateral volume of coro-nal dentine, including the lateral coronal aspect of thepulp chamber (mm3); LSEDJ, the enamel-dentine junction(EDJ) lateral surface (mm2); 3D LAET (= LVe/LSEDJ), thethree-dimensional lateral average enamel thickness (mm);3D LRET (= 100*3D LAET/(LVcdp1/3)), the scale-free three-dimensional lateral relative enamel thickness. Intra- andinterobserver tests for measurement accuracy run at dif-ferent times by four observers revealed differences < 4%. Forthe taxa with N > 1, we have firstly computed the LETDI foreach dm2/M1 pair and then calculated the average value.

Pearson correlation tests among the variables listedabove show that, in each molar pair, the 3D lateral rel-ative enamel thickness (3D LRET) exhibits the highestcorrelation (p < 0.01 vs. p < 0.02 for 3D LAET and p < 0.05for LVE). A “lateral enamel thickness diphyodontic index”(LETDI) has been thus calculated as follows: 3D LRETdm2/3DLRETM1. Statistical analyses were performed with R v.3.2.1(R Development Core Team, 2017).

To visualize similarities vs. differences in enamel thick-ness topography within an assemblage of such variablysized and shaped teeth, ad hoc imaging techniques wereused to virtually unroll lateral enamel and to project itinto standardized morphometric maps (Bayle et al., 2011;Bondioli et al., 2010; Macchiarelli et al., 2013; for simi-lar imaging techniques, see also Dowdeswell et al., 2017;Morita et al., 2016, 2017; Puymerail, 2011; Puymerail et al.,2012a, 2012b; Tsegai et al., 2017). Because each morpho-metric map (MM) is scaled according to the maximal valueof the analysed tooth, the patterns expressed by the dm2sand the M1s are independent from the absolute and rel-ative enamel thickness values. By using a custom routinedeveloped in R v.3.2.1 (R Development Core Team, 2017)with the packages spatstat (Baddeley et al., 2015) and gstat(Pebesma, 2004), enamel thickness values were standard-ized between 0 and 1 and each morphometric map wasset within a grid of 40 columns and 180 rows. We thenperformed a between-group principal component analy-sis (bgPCA; Mitteroecker and Bookstein, 2011) based onthe standardized morphometric map outputs with thepackage Morpho v.2.4.1.1 (Schlager, 2017) for R v.3.3.3 (RDevelopment Core Team, 2017).

3. Results

The scatterplot of the lateral relative enamel thicknessof the dm2 (3D LRETdm2) against the M1 values (3D LRETM1)of all individual and composite (Oreopithecus) tooth pairsused in this study is shown in Fig. 1. We observe little varia-tion among the four extant hominid genera, Gorilla and Pan

tending to align with the regression line, whereas Pongo

and humans scatter slightly more on both side of this line.Globally, the fossil taxa do not deviate much more than theextant hominids, Australopithecus and Paranthropus beingas distant from the regression line as the farthest extanthuman are. In this context, the composite individual rep-resenting Oreopithecus behaves like Pan.

For the ten hominid taxa, the 3D LRET values and thoseof the LETDI “diphyodontic index” are shown in Table 2.For the LRETdm2, Ouranopithecus (12.0), Paranthropus andthe Australopithecus from Sterkfontein (both 10.9) showabsolutely thick enamel, while Pongo and Gorilla (globalrange: 4.7–6.3) and Oreopithecus (6.0) are relatively thin-enamelled. A difference was noticeable between the twoAfrican apes, Pan having thicker enamel (6.3–8.9), buton average still thinner than measured in extant humans(8.0–9.2). Enamel in Neanderthals is thinner compared tothe extant values (6.4–7.1). As a whole, the decreasingorder for the lateral relative enamel thickness of thelower dm2 is as follows: Ouranopithecus > Paranthropus

= Australopithecus > extant humans ≥ Pan ≈ Neanderthals >Oreopithecus > Gorilla ≈ Pongo, the variation interval cov-ered by 3D LRET being comprised between 12.0 and 4.7.

Three sets are identifiable for the 3D LRETM1: the firstdistinguishes the absolutely thickly-enamelled Paran-

thropus (15.6) and Ouranopithecus (13.4), the secondassembles the variably intermediate Homo (all taxa), Pan,Australopithecus and Oreopithecus (range: 8.3–11.8), whilethe third includes the thinly-enamelled Gorilla and Pongo

(range: 5.9–8.1). In this context, Pan (8.8–11.8) is indistin-guishable from the extant human condition (9.3–11.2). TheNeanderthal range (8.3–9.1) fits the value obtained for Ore-

opithecus (9.2). Here, the decreasing pattern is as follows:Paranthropus > Ouranopithecus > Australopithecus ≥ extanthumans ≈ Pan ≥ Oreopithecus ≈ Neanderthals > Gorilla ≈

Pongo, the values globally ranging from 15.6 to 5.9.The last column of Table 2 presents the values of the

LETDI ratio. LETDI ranges in the whole sample from 0.63in a Pongo individual and 0.65 in Oreopithecus, to 0.98 inAustralopithecus and 0.99 in an extant human (Fig. 2). Thetotality of the ratios are < 1.0. According to this param-eter, even if distinct for its greater amount of enamel,Paranthropus (0.70) is closer to Oreopithecus (0.65) thanto Ouranopithecus (0.89), with which it otherwise sharesthickly-enamelled dm2 and M1. Within our limited set ofinvestigated cases, Pongo and extant humans display largervariation than Neanderthals and the African apes (Fig. 2).

Distinctly for each taxon and for each molar type, thestandardized morphometric maps (MM) imaging the vir-tually unrolled and projected lateral enamel are shown inFig. 3. For the extant taxa and Neanderthals, they repre-sent consensus maps generated by merging the availableindividual records into a single dataset and subsequentlycalculating the interpolation (Puymerail, 2011; Puymerailet al., 2012a, 2012b). Because each MM is scaled accordingto the maximal value of the analysed tooth, the patternsexpressed by the dm2s and the M1s are independent fromthe absolute and relative enamel thickness values.

In all taxa and both molars, enamel decreases cervi-cally. For the dm2, thickening is commonly found buccally;however, thickening in Ouranopithecus is more evenlydistributed around most of the subocclusal contour. Theextant human pattern is close to that displayed by theNeanderthal deciduous molars. The African apes and, to alesser extent, Pongo as well, share similar enamel distri-bution. In this context, the least contrasted map is that ofParanthropus, which is distinct from Australopithecus and,mostly, from Ouranopithecus, but which in turn recalls that

706 C. Zanolli et al. / C. R. Palevol 16 (2017) 702–714

Fig. 1. Scatterplot of the 3D lateral relative enamel thickness values of the dm2 (3D LRETdm2) against the M1 (3D LRETM1) comparatively assessed infour extant (HOM, PAN, GOR, PON) and five fossil hominid taxa (Nea, PAR, AUS, OUR, ORE). The red line represents the regression line of the 3D LRETdm2

against 3D LRETM1 . AUS: Australopithecus (africanus); GOR: Gorilla (sp.); HOM: extant humans; Nea: Neanderthals; ORE: Oreopithecus (bambolii); OUR:Ouranopithecus (macedoniensis); PAN: Pan (sp.); PAR: Paranthropus (robustus); PON: Pongo (sp.).Fig. 1. Graphique représentant l’indice tridimensionnel d’épaisseur relative de l’émail latéral des dm2s (3D LRETdm2) en fonction des M1s (3D LRETM1)pour quatre genres hominidés actuels (HOM, PAN, GOR, PON) et cinq taxons fossiles (Nea, PAR, AUS, OUR, ORE). La ligne rouge représente la droite derégression de 3D LRETdm2 en fonction de 3D LRETM1 . AUS : Australopithecus (africanus) ; GOR : Gorilla (sp.) ; HOM : humains actuels ; Nea : Néandertaliens ;ORE : Oreopithecus (bambolii) ; OUR : Ouranopithecus (macedoniensis) ; PAN : Pan (sp.) ; PAR : Paranthropus (robustus) ; PON : Pongo (sp.).

of Oreopithecus. In the MMs of the M1s, thickening is notmainly concentrated buccally, as seen for the dm2s, butmore commonly spread buccally/mesiobuccally and alsolingually/distolingually. However, this is not exactly thecase in Ouranopithecus and, to a lesser extent, in Oreop-

ithecus, where thickening is essentially concentrated mesi-olingually, in the former, and distolingually, in the latter.All extant and extinct human representatives show a simi-lar pattern resembling that of Australopithecus. Here again,the signatures displayed by the African apes are similar tothe pattern revealed by Pongo, which in turn recalls that ofParanthropus. Finally, in terms of intertooth polarity of thesignal, the most similar MMs are those of the extant apes(notably Gorilla and Pongo), while distinct topographic dif-ferences are appreciable in Paranthropus and Oreopithecus.

The bgPCA based on the MM scores only provides mod-est discrimination among the taxa along both bgPC axes(PC1: 56.37%, PC2: 31.11%). However, the representativesof all extant and fossil hominins (HOM, Nea, PAR, AUS) tendto regroup on the positive aspect of bgPC1, whereas the

extant apes (PAN, GOR and PON) mostly fall in the negativevalues along this axis (Fig. 4). The two Miocene hominids(OUR and ORE) show distinct signals, Ouranopithecus beingintermediate between Pongo and Homo, while Oreopithecus

more closely resembles Gorilla. The specimens in the posi-tive space of bgPC1 display evenly spread relatively thickerenamel deposited towards the more occlusal portion of theentire surface, while the specimens in the negative spaceof bgPC1 have two vertically projected thickened “pillars”on the buccal and lingual aspects, respectively, separatedby two large strips of thinner enamel nearly covering theentire mesial and distal crown sides. Along bgPC2, taxo-nomic discriminations are weak (Fig. 4).

The correlation between LETDI and body mass is shownin Fig. 5. Varying from good (notably in extant humans,but also in Neanderthals, Pan and Ouranopithecus) to mod-est (in Gorilla, Pongo and Paranthropus), a certain linearagreement is detectable in both smaller- and larger body-sized taxa. However, even ignoring the perhaps biasedsignal from the Oreopithecus composite representative, also

C. Zanolli et al. / C. R. Palevol 16 (2017) 702–714 707

Table 2

Three-dimensional lateral relative enamel thickness (3D LRET) of the second deciduous (dm2) and the first permanent (M1) lower molars and “lateral enamelthickness diphyodontic index” (LETDI: 3D LRETdm2/3D LRETM1) comparatively assessed in four extant (HOM, PAN, GOR, PON) and five fossil hominid taxa(Nea, PAR, AUS, OUR, ORE). In parentheses, the number of examined molar pairs.Tableau 2

Indice tridimensionnel d’épaisseur relative de l’émail latéral (3D LRET) des deuxièmes molaires déciduales (dm2) et des premières molaires permanentes(M1) inférieures et « indice diphyodonte d’épaisseur de l’émail latéral » (LETDI : 3D LRETdm2/3D LRETM1) comparés chez quatre genres hominidés actuels(HOM, PAN, GOR, PON) et cinq taxons fossiles (Nea, PAR, AUS, OUR, ORE). Le nombre de paires de molaires examinées est indiqué entre parenthèses.

Taxon 3D LRETdm2 3D LRETM1 LETDI

HOM Mean 8.4 10.4 0.81Range (5) 8.0–9.2 9.3–11.2 0.74–0.99

Nea Mean 6.7 8.8 0.76Range (3) 6.4–7.1 8.3–9.1 0.70–0.85

PAN Mean 7.5 10.1 0.74Range (4) 6.3–8.9 8.8–11.8 0.67–0.77

GOR Mean 5.4 6.9 0.79Range (5) 4.7–6.3 5.9–8.1 0.73–0.86

PON Mean 5.0 7.2 0.72Range (4) 4.8–5.3 5.9–8.0 0.63–0.90

PAR 10.9 15.6 0.70AUS 10.9 11.1 0.98OUR 12.0 13.4 0.89ORE 6.0 9.2 0.65

AUS: Australopithecus (africanus); GOR: Gorilla (sp.); HOM: extant humans; Nea: Neanderthals; ORE: Oreopithecus (bambolii); OUR: Ouranopithecus (mace-

doniensis); PAN: Pan (sp.); PAR: Paranthropus (robustus); PON: Pongo (sp.).

Fig. 2. Boxplots of the “lateral enamel thickness diphyodontic index” (LETDI) comparatively assessed in four extant (HOM, PAN, GOR, PON) and five fossilhominid taxa (Nea, PAR, AUS, OUR, ORE). AUS: Australopithecus (africanus); GOR: Gorilla (sp.); HOM: extant humans; Nea: Neanderthals; ORE: Oreopithecus

(bambolii); OUR: Ouranopithecus (macedoniensis); PAN: Pan (sp.); PAR: Paranthropus (robustus); PON: Pongo (sp.). The boxplot shows the median, the range(lower and upper whisker), the first quartile (lower hinge) and the last quartile (upper hinge).Fig. 2. Graphique illustrant le degré de variation de « l’indice diphyodonte d’épaisseur de l’émail latéral » (LETDI) estimé chez quatre genres d’hominidésactuels (HOM, PAN, GOR, PON) et cinq taxons fossiles (Nea, PAR, AUS, OUR, ORE). AUS : Australopithecus (africanus) ; GOR : Gorilla (sp.) ; HOM : humainsactuels ; Nea : Néandertaliens ; ORE : Oreopithecus (bambolii) ; OUR : Ouranopithecus (macedoniensis) ; PAN : Pan (sp.) ; PAR : Paranthropus (robustus) ;PON : Pongo (sp.). Les boîtes à moustaches montrent la médiane, les limites de variation (moustaches inférieure et supérieure), le premier quartile (partieinférieure de la boite) et le dernier quartile (partie supérieure de la boîte).

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Fig. 3. Standardized morphometric maps of the lateral enamel thickness of the dm2 (left column) and M1 (right) in four extant (HOM, PAN, GOR, PON)and five fossil hominid taxa (Nea, PAR, AUS, OUR, ORE) rendered by a chromatic scale ranging from thin (blue) to thick (red). For the extant taxa andNeanderthals, the consensus maps representing the “average” condition are shown. AUS: Australopithecus (africanus); GOR: Gorilla (sp.); HOM: extanthumans; Nea: Neanderthals; ORE: Oreopithecus (bambolii); OUR: Ouranopithecus (macedoniensis); PAN: Pan (sp.); PAR: Paranthropus (robustus); PON: Pongo

(sp.); m: mesial; d: distal.Fig. 3. Cartographies morphométriques standardisées de l’épaisseur de l’émail latéral des dm2 (colonne de gauche) et des M1 (colonne de droite) chezquatre genres d’hominidés actuels (HOM, PAN, GOR, PON) et cinq taxons fossiles (Nea, PAR, AUS, OUR, ORE) représentées par une échelle chromatiqueallant d’un émail fin (bleu) à épais (rouge). Pour les taxons actuels et les Néandertaliens, les cartes consensus représentant la condition « moyenne » sontillustrées. AUS : Australopithecus (africanus) ; GOR : Gorilla (sp.) ; HOM : humains actuels ; Nea : Néandertaliens ; ORE : Oreopithecus (bambolii) ; OUR :Ouranopithecus (macedoniensis) ; PAN : Pan (sp.) ; PAR : Paranthropus (robustus) ; PON : Pongo (sp.) ; m : mésial ; d : distal.

Australopithecus behaves here as an outlier, a result whichdeserves confirmation from the inclusion in the analy-sis of the signal from additional individuals. Interestingly,extant humans and Gorilla, which display comparable aver-age LETDIs, differ in average body mass and the twolargest-sized taxa considered in our analysis, Gorilla andOuranopithecus, provided distinct LETDI ratios.

4. Discussion

A limiting/complicating factor in our analyticalapproach is the use of non-occlusal enamel compared tothe information imprinted occlusally, or even at specificcuspal level (e.g., Grine, 2005; Kono et al., 2002; Machoand Berner, 1993; Mahoney, 2010; Schwartz, 2000b).However, lateral enamel has its own signals that havenever been previously explored as a functional unit

independent of occlusal enamel thickness. In this sense,our study attempts to do this for the first time. Whileocclusal enamel topography is more directly informativein terms of functional activity and adaptive responses(e.g., Guy et al., 2013; Kono, 2004; Kono and Suwa, 2008;Olejniczak et al., 2008b), lateral enamel thickness is alsoinvolved in dissipating occlusally-related stresses (Benazziet al., 2013a, 2013b). Lateral enamel also resists wear,tooth height loss and maintains interproximal tooth-toothcontacts during the late stages of tooth wear after dentineexposure over the occlusal surface. Final loss of lateralenamel marks the breakdown of the dentition (Dean et al.,1992) and is significant in the life history of individuals.Nonetheless, it is also possible that the use of the entirelyunrolled lateral crown band introduced inessential, oreven somehow noisy information. In fact, while individualmorphometric maps clearly reveal site-specific differences

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Fig. 4. bgPCA plot based on the standardized morphometric maps (MM) of the dm2 and M1 of four extant (HOM, PAN, GOR, PON) and five fossil hominid taxa(Nea, PAR, AUS, OUR, ORE). The MMs below the plot show the extreme conditions along bgPC1 and bgPC2. AUS: Australopithecus (africanus); GOR: Gorilla

(sp.); HOM: extant humans; Nea: Neanderthals; ORE: Oreopithecus (bambolii); OUR: Ouranopithecus (macedoniensis); PAN: Pan (sp.); PAR: Paranthropus

(robustus); PON: Pongo (sp.); m: mesial; d: distal.Fig. 4. Graphique bgPCA basé sur les cartes morphométriques standardisées (MM) des dm2 et M1 chez quatre genres d’hominidés actuels (HOM, PAN,GOR, PON) et cinq taxons fossiles (Nea, PAR, AUS, OUR, ORE). Les MM sous le graphique montrent les conformations extrêmes le long de bgPC1 et bgPC2.AUS : Australopithecus (africanus) ; GOR : Gorilla (sp.) ; HOM : humains actuels ; Nea : Néandertaliens ; ORE : Oreopithecus (bambolii) ; OUR : Ouranopithecus

(macedoniensis) ; PAN : Pan (sp.) ; PAR : Paranthropus (robustus) ; PON : Pongo (sp.) ; m : mésial ; d : distal.

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Fig. 5. Values of the “lateral enamel thickness diphyodontic index” (LETDI) compared with body mass estimates (average values, from Fleagle, 2013) in fourextant (HOM, PAN, GOR, PON) and five fossil hominid taxa (Nea, PAR, AUS, OUR, ORE). The red line represents the regression line of the body mass against theLETDI. AUS: Australopithecus (africanus); GOR: Gorilla (sp.); HOM: extant humans; Nea: Neanderthals; ORE: Oreopithecus (bambolii); OUR: Ouranopithecus

(macedoniensis); PAN: Pan (sp.); PAR: Paranthropus (robustus); PON: Pongo (sp.).Fig. 5. Valeurs de « l’indice diphyodonte d’épaisseur de l’émail latéral » (LETDI) comparées aux estimations de masse corporelle (valeurs moyennes, d’aprèsFleagle, 2013) pour quatre genres d’hominidés actuels (HOM, PAN, GOR, PON) et cinq taxons fossiles (Nea, PAR, AUS, OUR, ORE). La ligne rouge représentela droite de régression de la taille corporelle en fonctions de l’indice LETDI. AUS : Australopithecus (africanus) ; GOR : Gorilla (sp.) ; HOM : humains actuels ;Nea : Néandertaliens ; ORE : Oreopithecus (bambolii) ; OUR : Ouranopithecus (macedoniensis) ; PAN : Pan (sp.) ; PAR : Paranthropus (robustus) ; PON : Pongo

(sp.).

among the compartments which relate to occlusal cuspshape and topography (Fig. 3), at this stage we did notyet decompose the band into its mesial, distal, buccal andlingual components, and did not examine and comparetheir sometimes distinctly heterogeneous signatures. Thistask we would expect to limit the effects of differences intooth crown architecture, notably outer surface convexityand intercuspal groove depth and extension. This, will inany case require additional research and the developmentof ad hoc analytical protocols, also because the outlineshape of the dm2s and M1s used in this study tends todiffer and, notably in the case of intertaxonomic analysesusing variably-shaped tooth crowns, a risk of comparingnot exactly homologous spots exists.

The expectation, formulated in a purely functional per-spective, of LETDI ratios < 1.0 (the M1 crown being in princi-ple equipped with a thicker coating of enamel for resistinghigher and prolonged wear-inducing loads) is not fullysatisfied by the present results (for enamel proportionsin extant human lower dm1s-dm2s-M1s, see Mahoney,

2010). In two representatives from as many taxa it is closeto be falsified: an extant human individual (0.99), and theAustralopithecus representative (0.98), even if the largemajority of the ratios are around or below 0.8. The two min-ima for the LETDI correspond to Oreopithecus (0.65, a valueobtained from two individuals, thus prone to bias) andParanthropus (0.70). This is interesting, and may be relevantwhenever confirmed by additional data, as it might indi-cate that a large difference between the dm2 and the M1in the proportional amount of enamel volume depositedalong the crown walls occurs in both absolutely thickly-enamelled and relatively thinly-enamelled hominids. Inany case, the results (Table 2, Fig. 2) show also that theopposite can occur, i.e., that the deciduous and permanentmolars of both thickly-enamelled hominids (e.g., Ouranop-

ithecus) and representatives of relatively thinly-enamelledtaxa (e.g., Gorilla, Pongo) may present comparable values oflateral relative enamel thickness (3D LRET). In sum, even ifpresent results tend to support the evidence that primate“deciduous teeth have thinner enamel than permanent

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teeth” (Swindler, 2002: 14), including in humans(Mahoney, 2010), the extent of their enamel proportions,at least for non-occlusal enamel, appears rather variable.

By definition, the study assumed that the signal revealedby each dm2-M1 crown pair represents the averagecondition of their own taxon (including for the compos-ite Oreopithecus representative). However, even if molarenamel thickness does not seem to behave as sexuallydimorphic (e.g., Hlusko, 2016; Hlusko et al., 2004; Rossiet al., 1999), a growing body of evidence indicates aconsiderable amount of interspecific temporal and geo-graphic variation (e.g., Kato et al., 2014; Smith et al.,2011, 2012). Conversely, the extent of intraspecific vari-ation ranges in most cases from poorly reported to simplyunknown, and even in extant humans enamel thicknesschrono-geographic variation is far from being appropri-ately documented (Le Luyer and Bayle, 2017) and, withvery few exceptions (e.g., Feeney et al., 2010; Grine, 2005),most currently available information is limited to Euro-pean or European-derived population samples (rev. in LeLuyer, 2016; see Zanolli et al., 2017). At any rate, thepresent evidence based on the limited number of Africanapes represented here suggests variation in lateral enamelthickness may be similarly large in both deciduous andpermanent molars (Table 2).

To interpret the “lateral enamel thickness diphyodon-tic index” more comprehensively – or indeed any otherkind of “enamel thickness diphyodontic index” (ETDI) suit-able for appropriately assessing the deciduous-permanenttooth enamel volume proportions (and its distribution pat-tern as well) – a number of biological, behavioural andecological factors should be taken into account.

The four extant and four extinct hominid genera rep-resented in our analysis are known for exploiting, or arereported to have exploited, respectively, a wide rangeof food resources in a variety of diverse environments(Fleagle, 2013; Guatelli-Steinberg, 2016; Hartwig, 2002;Merceron et al., 2005; Nelson and Rook, 2016; Scott et al.,2005; Sponheimer and Lee-Thorp, 2015; Ungar, 2007;Ungar and Sponheimer, 2013). Depending on the taxon-specific feeding habits, the time spent feeding may beconsidered as another variable which, together with foodabrasiveness, likely plays a role in the selection of enamelthickness because of dental wear resistance, i.e., adapta-tion is not only resistance to fracture, but also to prolongedperiods of wear to which enamel thickness can be related(Grine and Daegling, 2017; Pampush et al., 2013). Theinvestigative tool used here – the LETDI – did not reveal anyimmediately obvious link with known dietary and/or eco-logical niche; for example, relative medium-low (< 0.80)values are shared by Neanderthals, Pan, Gorilla, Pongo,Paranthropus and Oreopithecus, while extant humans, Aus-

tralopithecus and Ouranopithecus provided medium-highvalues (> 0.80). We note, anyhow, that in the bgPCA ofthe morphometric maps (Fig. 4): the more folivorous taxa(Pan, Gorilla, and perhaps Oreopithecus) tend to be in thenegative space of bgPC1; Pongo, a slightly more diversi-fied folivorous/frugivorous feeder, is found in the positivespace of bgPC1; the omnivorous humans are mostly scat-tered across the positive space of bgPC1 and the positivespace of bgPC2; Paranthropus and Australopithecus, which

likely also with Ouranopithecus relied on diverse diets butshared the inclusion of hard/gritty food items, are foundin the positive part of bgPC1, but scattered along bgPC2(Fig. 4); finally, Ouranopithecus sets in the negative space ofbgPC2, the dm2 and M1 being spread along the bgPC1 axis.In sum, even if we agree the reliability of enamel thicknessas a dietary indicator breaks down in some cases wherephylogenetically closely-related species that consume dif-ferent amounts of hard items are considered (Grine andDaegling, 2017), at a first glance, differences in “dentalecology” (sensu Cuozzo et al., 2012) seem to play a rolein affecting the polarity of the dm2/M1 ratio used in thepresent study. If so, additional research – using any kind ofad hoc ETDI – should be performed on the anterior teeth.

The taxa investigated here are also diverse in body mass(Fleagle, 2013; Hemmer, 2015), a variable that in extantprimates is correlated to a number of life history attributes(e.g., weaning age, age at maturity, age at first breedingin females), as well as to tooth size (e.g., molar crownarea) (rev. in Hemmer, 2015). Even if our current analysescomparing LETDI with body size only shows limited lin-ear correlation between these variables, it still representsa promising research track for the future.

Our “diphyodontic index” seems to be poorly or notrelated to the age at eruption of the first lower perma-nent molar, another key life history trait which in homininsmarks the end of infancy (Kelley and Bolter, 2013). In fact,while also a strong genetic contribution to variation in tim-ing of primary tooth emergence is well documented inhumans (Chan et al., 2012), and likely also in hominids(Swindler, 2002), the LETDIs of Pan and of the Australop-

ithecus representative used here that, for example, showcomparable ages at LM1 eruption (Hemmer, 2015: table15), differ markedly.

5. Concluding remarks

In a previous study, we noted that “some evidence sug-gests deciduous versus permanent molar enamel thicknessdistribution and relative proportions vary among extantand fossil hominid taxa. . . Inner signatures extracted fromthe primary and secondary dentition, respectively, mayor may not provide similar/comparable pictures of time-related intrataxic evolutionary changes in tooth tissueproportions” (Macchiarelli et al., 2013: 259). The resultscollected from the present exploratory test using a newlydeveloped analytical tool – the “lateral enamel thicknessdiphyodontic index” (LETDI) – did not, however, provide anunambiguous and immediately readable picture, as mightotherwise have been predictable on the basis of someontogenetic and morphological studies using sequentialteeth (e.g., Bailey et al., 2014, 2016; Evans et al., 2016).Rather, our results suggest complex patterns that likelyresult from the influence of a number of interactive fac-tors. Increasing evidence exists for lifetime-related enamelthickness and dietary wear association in extant primates(e.g., Pampush et al., 2013) and positive selection for adap-tation in human evolution has been shown for the genescoding for the enamel matrix proteins (e.g., Daubert et al.,2016; Horvath et al., 2014). However, given also the highphenotypic plasticity of enamel thickness (e.g., Hlusko,

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2016; Kato et al., 2014; Smith et al., 2012), it is possiblethat a fraction of the signal provided by any kind of toothenamel “diphyodontic index” is non-adaptive, or that thedegree of adaptability and functional significance of thistrait varies topographically across the dentition. With thisrespect, together with some methodological advancementin the identification of the most reliable parameters andtooth crown areas to be considered for intertaxonomicinvestigations, a fruitful area of research would be to testthe congruence of the “diphyodontic signal” between theanterior and the postcanine dentition, as well as betweenenamel and the enamel-dentine junction topography.

Acknowledgements

The present study contributes to the Palevol thematicissue “Hominin biomechanics, virtual anatomy and innerstructural morphology: From head to toe. A tribute to Lau-rent Puymerail”, promoted by C.Z. and R.M. Our friendand colleague Laurent was among the developers of the“unrolling” routine used in this study, and also pro-vided relevant conceptual inputs. With his innovative andthoughtful work, only developed along a terribly shorttime, Laurent marked the field of “virtual palaeoanthro-pology”. We acknowledge also his elegant style and sharpintellect. We really miss him.

For having granted or facilitated the access to thematerials used in this study, we are very grateful to J.-J. Cleyet-Merle (Les Eyzies-de-Tayac), L. de Bonis (Poitiers),D. Grimaud-Hervé (Paris), G. Koufos (Thessaloniki), S. Potze(Pretoria), L. Rook (Florence), F. Sémah (Paris), F. Thackeray(Johannesburg), J.-F. Tournepiche (Angoulême), L. Trebini(Sassari), H. Widianto (Jakarta), M.D. Wandhammer (Stras-bourg). The microtomographic records of the specimensdetailed outside the platform set at the Univ. of Poitiershave been realized thanks to the support provided byA. Bravin (Grenoble), F. de Beer (Pelindaba-Johannesburg),J. Hoffman (Pelindaba-Johannesburg), B. Illerhaus (Berlin),C. Nemoz (Grenoble), P. Tafforeau (Grenoble). For dis-cussion, we acknowledge D.M. Alba (Barcelona), J. Braga(Toulouse), F.E. Grine (Stony Brook), J. Kelley (Tempe),L. Rook (Florence).

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